Intestine-to-germline transmission of epigenetic information transgenerationally ensures systemic stress resistance in C. elegans
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PROVIDER: PRJNA490709 | ENA |
REPOSITORIES: ENA
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Project description:Epigenetic states are metastable and changed throughout life, and their changes play a major role in the regulation of organismal homeostasis, including stress resistance. However, the mechanisms coordinating epigenetic states and systemic stress resistance across tissues remain largely unknown. Here, we identify the intestine-to-germline communication of epigenetic states, which enhances stress resistance transgenerationally in C. elegans. We firstly show that the alteration in epigenetic states by deficiency of the histone H3K4me3 modifier ASH-2 in the intestine or germline increases organismal oxidative stress resistance, which is abrogated by knockdown of the H3K4 demethylase RBR-2 in the same tissue. Remarkably, the increase in stress resistance induced by ASH-2 deficiency in the intestine is abrogated by RBR-2 knockdown in the germline, suggesting the existence of inter-tissue transmission of epigenetic information from intestine to germline. Simultaneously, this intestine-to-germline communication in the parental generation transgenerationally provides the increase in stress resistance of the descendants for over two generations. Further analyses reveal that the inter-tissue communication requires the insulin/IGF-1 signaling effector DAF-16/FOXO in the intestine and is mediated, at least in part, by transcriptional regulation of F08F1.3, one of the intestinal ASH-2 target genes. These results unveil the novel intestine-to-germline communication of epigenetic information that provides the transgenerational regulation of organismal stress resistance. To further investigate the molecular mechanisms underlying intestine-to-germline communication, we sought the gene expression changes in the intestine ash-2 knockdown worms.
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Project description:It is unknown whether the activity of the nervous system can be inherited. In Caenorhabditis elegans nematodes, parental responses can transmit heritable small RNAs that regulate gene expression transgenerationally. In this study we show that a neuronal process can impact the next generations. Neurons-specific synthesis of RDE-4-dependent small RNAs regulates germline amplified endogenous siRNAs and germline gene expression for multiple generations. Further, the production of small RNAs in neurons controls the chemotaxis behavior of the progeny for at least three generations via the germline Argonaute HRDE-1. Among the targets of these small RNAs we identified the conserved gene saeg-2, which is transgenerationally downregulated in the germline. Silencing of saeg-2 following neuronal small RNA biogenesis is required for chemotaxis under stress. Thus, we propose a small RNA-based mechanism for communication of neuronal processes transgenerationally.
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